Flowering of Arabidopsis is regulated by several environmental and endogenous signals. An important integrator of these inputs is the FLOWERING LOCUS T (FT) gene, which encodes a small, possibly mobile protein. A primary response to floral induction is the activation of FT RNA expression in leaves. Because flowers form at a distant site, the shoot apex, these data suggest that FT primarily controls the timing of flowering. Integration of temporal and spatial information is mediated in part by the bZIP transcription factor FD, which is already expressed at the shoot apex before floral induction. A complex of FT and FD proteins in turn can activate floral identity genes such as APETALA1 (AP1).
Plants are responsive to temperature, and can distinguish differences of 1ºC. In Arabidopsis, warmer temperature accelerates flowering and increases elongation growth (thermomorphogenesis). The mechanisms of temperature perception are however largely unknown. We describe a major thermosensory role for the phytochromes (red light receptors) during the night. Phytochrome null plants display a constitutive warm temperature response, and consistent with this, we show in this background that the warm temperature transcriptome 2 becomes de-repressed at low temperatures. We have discovered phytochrome B (phyB) directly associates with the promoters of key target genes in a temperature dependent manner.The rate of phyB inactivation is proportional to temperature in the dark, enabling phytochromes to function as thermal timers, integrating temperature information over the course of the night. One Sentence Summary:The plant temperature transcriptome is controlled at night by phytochromes, acting as thermoresponsive transcriptional repressors. Main Text:Plant development is responsive to temperature, and the phenology and distribution of crops and wild plants have already altered in response to climate change (1, 2). In Arabidopsis thaliana, warm temperature-mediated elongation growth and flowering is dependent on the bHLH transcription factors PHYTOCHROME INTERACTING FACTOR4 and 5 (PIF4 and 5) (3-6). Growth at 27ºC reduces the activity of the Evening Complex (EC) resulting in greater PIF4 transcription. The EC is a transcriptional repressor made up of the proteins EARLY FLOWERING3 (ELF3), ELF4 and LUX ARRHYTHMO (LUX) (7-9). To test if the EC is also required for hypocotyl elongation responses below 22ºC, we examined the behavior of elf3-1 and lux-4 at 12 and 17ºC. Hypocotyl elongation in elf3-1 and lux-4 is largely suppressed at lower temperatures (Fig. 1A, B), which is consistent with cold temperatures being able to suppress PIF4 overexpression phenotypes (10). Since PHYTOCHROME B (PHYB) was identified as a QTL for thermal responsiveness and PIF4 activity is regulated by phytochromes (8, 11), we investigated whether these red light receptors control hypocotyl elongation in the range 12 to 22ºC. Plants lacking phytochrome activity (12) show constitutively long hypocotyls at 12ºC and 17ºC. Thus phytochromes are essential for responding to temperature (Fig. 1C, D and Fig. S1).We used transcriptome analysis to determine whether disrupted thermomorphogenesis in phyABCDE is specific for temperature signaling or is a consequence of misregulated growth pathways. To capture diurnal variation in thermoresponsiveness, we sampled seedlings over 24 hours at 22 and 27ºC. Clustering analysis reveals 20 groups of transcripts ( Fig. 2A and Fig. S3; described in supplement). Thermomorphogenesis occurs predominantly at night and is driven by PIF4. Consistent with this, we observe PIF4 is present in cluster 20, which is more highly expressed at 27ºC during darkness. Clusters 15 and 16 represent the other major groups of 3 nighttim...
Plants are sessile organisms and must respond to changes in environmental conditions. Flowering time is a key developmental switch that is affected by both day length and temperature. Environmental cues are sensed by the leaves while the responses occur at the apex, requiring long-range communication within the plant. For many years it has been known that leaves exposed to light can trigger the floral transition of a darkened shoot, and grafting experiments demonstrated that the floral stimulus travels long distances. This mobile signal was later termed "florigen," but its nature has been unclear. The gene FLOWERING LOCUS T (FT) is a major output of both the photoperiod and the vernalization pathways controlling the floral transition. FT protein acts at the shoot apex of the plant in concert with a transcription factor, FLOWERING LOCUS D (FD). A fundamental question is how FT transcription in the leaves leads to active FT protein at the apex. We have uncoupled FT protein movement from its biological function to show that FT protein is the mobile signal that travels from the leaves to the apex. To our knowledge, FT is the only known protein that serves as a long-range developmental signal in plants.
Temperature is a major environmental variable governing plant growth and development, and climate change has already altered the phenology of wildplants and crops 1 . However, the mechanisms by which plants sense temperature are not well understood. Environmental signals, including temperature, are integrated into growth and developmental pathways via the circadian clock and the activity of the Evening Complex (EC), a major signalling hub and core clock component 2,3 . The EC acts as a temperature responsive transcriptional repressor, providing rhythmicity and temperature responsiveness to growth via unknown mechanisms 2,4-6 . The EC consists of EARLY FLOWERING3 (ELF3) 4,7 , a large scaffold protein and key component
Plant development is highly responsive to ambient temperature, and this trait has been linked to the ability of plants to adapt to climate change. The mechanisms by which natural populations modulate their thermoresponsiveness are not known. To address this, we surveyed Arabidopsis accessions for variation in thermal responsiveness of elongation growth and mapped the corresponding loci. We find that the transcriptional regulator EARLY FLOWERING3 (ELF3) controls elongation growth in response to temperature. Through a combination of modeling and experiments, we show that high temperature relieves the gating of growth at night, highlighting the importance of temperature-dependent repressors of growth. ELF3 gating of transcriptional targets responds rapidly and reversibly to changes in temperature. We show that the binding of ELF3 to target promoters is temperature dependent, suggesting a mechanism where temperature directly controls ELF3 activity.
Plants maximise their fitness by adjusting their growth and development in response to signals such as light and temperature. The circadian clock provides a mechanism for plants to anticipate events such as sunrise and adjust their transcriptional programmes. However, the underlying mechanisms by which plants coordinate environmental signals with endogenous pathways are not fully understood. Using RNA-seq and ChIP-seq experiments, we show that the evening complex (EC) of the circadian clock plays a major role in directly coordinating the expression of hundreds of key regulators of photosynthesis, the circadian clock, phytohormone signalling, growth and response to the environment. We find that the ability of the EC to bind targets genome-wide depends on temperature. In addition, co-occurrence of phytochrome B (phyB) at multiple sites where the EC is bound provides a mechanism for integrating environmental information. Hence, our results show that the EC plays a central role in coordinating endogenous and environmental signals in Arabidopsis.
Temperature is a major environmental cue affecting plant growth and development. Plants often experience higher temperatures in the context of a 24 h day-night cycle, with temperatures peaking in the middle of the day. Here we find that the transcript encoding the bHLH transcription factor PIF7 undergoes a direct increase in translation in response to warmer temperature. Diurnal expression of PIF7 transcript gates this response, allowing PIF7 protein to quickly accumulate in response to warm daytime temperature. Enhanced PIF7 protein levels directly activate the thermomorphogenesis pathway by inducing the transcription of key genes such as the auxin biosynthetic gene YUCCA8, and are necessary for thermomorphogenesis to occur under warm cycling daytime temperatures. The temperature-dependent translational enhancement of PIF7 mRNA is mediated by the formation of an RNA hairpin within its 5' UTR, which adopts an alternative conformation at higher temperature, leading to increased protein synthesis. We identified similar hairpin sequences that control translation in additional transcripts including WRKY22 and the key heat shock regulator HSFA2, suggesting this is a conserved mechanism enabling plants to respond and adapt rapidly to high temperatures.
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